Multiple predator effects & native prey behavioral responses to two Ashley E. Porter*1, Jennifer S. Rehage1, William F. Loftus2, and Shawn E. Liston3 1Oceanographic Center, Nova Southeastern University, Dania Beach, FL, USA*[email protected] non-native 2 non-native cichlids United States Geological Survey, Florida Integrated Science Center, Everglades National Park Field Station, Homestead, FL, USA 3Corkscrew Swamp Sanctuary, Audubon of Florida, Naples, FL, USA

Introduction Field-Enclosure Experiment Conclusions •Our results showed that the well-established invader had a larger predation effect Ecological systems contain multiple predators and prey but few studies have than the recent invader. Treatment, p=0.0096 •Mayan cichlids have a higher examined the complex interactions, especially with non-native predators. Prey •L. goodei was consumed 30 predation rate than African by Mayan cichlids, but •Both cichlids preyed selectively on J. floridae while Mayan cichlids also consumed may be evolutionary naïve with such predators and thus exhibit ineffective or NP No Predator Control jewelfish. avoided in African L. goodei. inappropriate defense behaviors when faced with a novel threat. Introduced- 25 jewelfish and adult Mayan mm 2 Mayan cichlids •The low recovery of H. formosa could be due to our difficulty in finding survivors predator effects may be attenuated or exacerbated depending on interactions •There was no evidence that -African jewelfish among the large volume of floc and periphyton in the cages. Alternatively, it may 20 prey experience a release from JJ 2 African jewelfish have been the result of predation of H. formosa by G. holbrooki. with native predators or with previously established non-native predators. tality treatment. r

o predation when both cichlids 15 M •J. floridae seemed to be consumed preferentially in the mixed-predator treatment are present. y •There was a complete mJ sub-adult Mayan cichlid More than 12 non-indigenous fish species are currently established in e when adult Mayans were present. That may indicate a potential risk enhancement 10 avoidance of G. holbrooki African jewelfish (Sih et al., 1998; Schmitz, 2007) if they experience higher mortality when exposed to Everglades National Park (ENP), a large number relative to the small 35-species •Predation rates were multiple predators versus only one predator (Sih et al., 1998). tal Pr across treatm ents. o unaffected by Mayan size. MJ adult Mayan cichlid native fish fauna. A recent biological invasion of ENP (ca. 2002) is that of the T 5 African jewelfish •Predation rates were similar between adult and sub-adult Mayan cichlids in African jewelfish, . Among the most abundant and •The recovery of P. agreement with Bergmann & Motta (2005) which showed no ontogenetic diet shifts. 0 •All predator combinations paludosus and H. formosa well-established non-native fishes is the Mayan cichlid, Cichlasoma NP mm JJ mJ MJ consumed J. floridae, was lowest in the control •Intraspecific interaction rates were higher for African jewelfish, which may relate urophthalmus. We used a field enclosure experiment to assess and compare particularly with adult Mayan to their lower predation rate, and result in a release from predation. Fig. 7. Total prey mortality for all prey combined. treatment. predation effects of these two non-native cichlids and an experiment cichlid-African jewelfish. •The habita t domain of the predators appeared to overlap but their predation tactics to examine predator tactics and anti-predator behavioral responses. differed. African jewelfish are active predators whereas Mayan cichlids appear to

have a sit-and-wait hunting style (Schmitz, 2007). Little interspecific interactions Treatment by Species, p=0.0013 were observed despite the fact that they overlap in domain, which could be 1.0 1.0 1.0 1.0 1.0 attributed to their difference in activity. J. floridae L. goodei G. holbrooki P. paludosus H. formosa 0.8 0.8 0.8 0.8 0.8 www.nativefish.org •The habitat domain of the predators overlapped with certain prey which were the most consumed by the predators. lpha Research Questions a 0.6 0.6 0.6 0.6 0.6 s • Are these two predators functionally redundant (i.e., are predation rates and ' •Prey showed significant behavioral variation in response to the two predators. preferences similar)? 0.4 0.4 0.4 0.4 0.4

• How do these predators interact (including as a function of size since Manly •Predators consumed prey that did not respond, and prey that responded indiscriminately to the predation threat. This indiscriminant response may have Mayan cichlids are larger)? 0.2 0.2 0.2 0.2 0.2 been ineffective. • How do native prey respond to these non-native predators? 0.0 • How does anti-predator behavior relate to the vulnerability to predation of 0.0 0.0 0.0 0.0 prey? NP mm JJ mJ MJ NP mm JJ mJ MJ NP mm JJ mJ MJ NP mm JJ mJ MJ NP mm JJ mJ MJ

Fig. 8. Prey selectivity indexes by prey species and treatment. The line indicates no preference (a Manly’s alpha value of 1/m = 0.2, where m= 5 prey items available).

Field Enclosure Experiment Implications

•We conducted an in situ replacement series experiment (Schmitz, 2007) in a This study provides insight into the nature of interactions between African jewelfish, Mayan cichlids, and the native Everglades aquatic- community. It ran domized-block design at the peak of the wet season (October 2007; mean water level 33.4 cm) to compare mortality rates. Laboratory Behavior Experiment is important to determine if predation by the non-native cichlids poses a 2.0 G. holbrooki Species (prey), p=<0.0001 formidable threat to the native community, and if range expansion by African Treatment, p=0.0007 NP H. formosa Treatments (single predators), p=0.0777 L. goodei Species, p=<0.0001 mm 3.0 jewelfish will result in negative impacts to areas of the Everglades presently JJ J. floridae Treatment by Species, p=0.0019 mJ P. paludosus uncolonized. Invasive species are a major conservation concern in the restoration MJ •Prey activity was highest in the absence H. letourneuxi 1.5 C. urophthalmus of the Everglades and may be affected indirectly by CERP actions. For instance, the of predators and lowest with African 2.5 projected removal of 386 km of canals and levees will remove canal habitat that is n ty i jewelfish. o i t v home to a number of non-native fish species, and that seem to be cold-temperature i

1.0 bu 2.0 refuges, allowing recolonization of marshes after severe winters. However, new ri

Act •J. floridae and P. paludosus lowered their st

i structures and canals are also planned to move water in CERP projects, and activity to all predators whereas G. ramifications for invasive species should be considered in that planning. Overall,

al D 1.5

holbrooki lowered activity to the African c Map courtesy of: Fig. 2. Enclosures were constructed i www.nps.gov 0.5 restoration should enhance Everglades habitats and the functional quality of the 2 rt of 1-m polypropylene mesh Fig. 3. Ambient floc & periphyton jewelfish.

Ve ecosystem, which has been shown by research to benefit native species to the Fig. 1. Map of lower ENP, green cubes attached to PVC frames as well as artificial steel stems arrow indicates study site (25° oriented in one row east to west, were added to the enclosures to 1.0 detriment of non-native taxa. 16.97’ N, 80° 47.88’ W). perpendicular to water flow. •H. formosa was more active in the provide habitat complexity. 0.0 G. holbrooki H. formosa L. goodei J. floridae P. paludosus presence of the adult Mayan cichlid- Species Fig. 9. Prey activity levels by treatment and species scored African jewelfish than in either of the Fig. 11. Vertical distribution of prey and predators by species in Laboratory Behavior Experiment as 2=active, 1=slightly active, and 0=not active. single-predator treatments. the water scored as 1=top, 2=middle, 3=bottom.

•Timed trials were conducted in aquaria with similar randomized-block design to record behavioral interactions. Six hourly spot-check observations were taken. •L. goodei did not respond to any Literature Cited Treatment, p=<0.0001 Treatment, p= <0.0001 Bergmann GT, Motta PJ (2005) Diet and morphology through ontogeny of the nonindigenous Mayan predator combinations. 1.0 2.0 cichlid Cichlasoma (Nandopsis) urophthalmus (Günter 1862) in southern Florida. Environmental

n Biology of Fishes 72: 205-211 0.8 io

•African jewelfish had the highest t Schmitz OJ (2007) Predator diversity and trophic interactions. Ecology 88: 2415-2426 c 1.5 a Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends in activity and inte raction rates. s ter r 0.6 2 Mayan cichlids adult Mayan cichlid Ecology and Evolution 13: 350-355 n

African jewelfish I •African jewelfish lowered activity when r

edato 1.0 0.4 r Mayan cichlids of either size were p edato f

o present. Pr Fig. 4. Variables recorded included prey & predator 2 African jewelfish sub-adult Mayan cichlid 0.5 0.2 ity activity and vertical distribution and predator African jewelfish + No Predator Control •Both predators overlapped in habitat Acknowledgments interactions. Habitat structure comprised 22% 0.0 volumetrically and water depth matched the field. Fig. 5. Treatments used in both experiments. Activ domain with J. floridae, L. goodei, and P. This project was funded by the Park-Oriented Biological Support Initiative of the 0.0 mm JJ mJ MJ mm JJ mJ MJ paludosus, but not G. holbrooki or H. U.S. Geological Survey, POBS 06-086). We wish to thank Everglades National Park formosa. especially J. Kline and P. J. Walker for permits and support of the study. The project Fig. 12. Predator interactions by treatment, scored as 0=no www.nativefish.org Fig. 10. Predator activity levels shown by treatment, scored interaction and 1=interaction. could not have been executed without the field assistance of K. Dunlop, L. Flagfish Eastern Mosquitofish Bluefin Killifish Riverine Grass Shrimp Least Killifish in the same way as prey species. Jordanella floridae Gambusia holbrooki Lucania goodei Palaemonetes paludosus Heterandria formosa McCarthy, and N. Katin, the collection and laboratory assistance of A. Whitaker, A. Fig. 6. Native prey; 6 individuals used for the field study and 2 individuals used for the aquaria study, per species. Hayden, and P.F. Rehage, and the field enclosures loaned by J.C. Trexler.